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The Blood Supply of the Large Intestine

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Journal of Anatomy
J. Anat. (2010) 216, pp335–343 doi: 10.1111/j.1469-7580.2009.01199.x

The spatial arrangement of the human large intestinal


wall blood circulation
David Kachlik,1,2 Vaclav Baca1,2 and Josef Stingl1
1
Third Faculty of Medicine, Charles University in Prague, Ruská, Praha, Czech Republic
2
Department of Medicine and Humanities, Faculty of Biomedical Engineering, Czech Technical University in Prague, Kladno,
Czech Republic

Abstract
The aim of the study was to describe and depict the spatial arrangement of the colon microcirculatory bed as a
whole. Various parts of the large intestine and terminal ileum were harvested from either cadaver or section
material or gained peroperatively. Samples were then injected with India ink or methylmetacrylate Mercox resin
for microdissection and corrosion casting for scanning electron microscopy. The results showed that extramural
vasa recta ramified to form the subserous plexus, some of them passing underneath the colon taeniae. Branches
of both short and long vasa recta merged in the colon wall, pierced the muscular layer and spread out as the
submucous plexus, which extended throughout the whole intestine without any interruption. The muscular
layer received blood via both the centrifugal branches of the submucous plexus and the minor branches sent
off by the subserous plexus. The mucosa was supplied by the mucous plexus, which sent capillaries into the
walls of intestinal glands. The hexagonal arrangement of the intestinal glands reflected their vascular bed. All
three presumptive critical points are only gross anatomical points of no physiological relevance in healthy indi-
viduals. Neither microscopic weak points nor regional differences were proven within the wall of the whole
large intestine. The corrosion casts showed a huge density of capillaries under the mucosa of the large intes-
tine. A regular hexagonal pattern of the vascular bed on the inner surface was revealed. No microvascular criti-
cal point proofs were confirmed and a correlation model to various pathological states was created.
Key words injection; large intestine; microcirculation; scanning electron microscopy.

(tela subserosa, subserous layer), muscular layer (tunica


Introduction
muscularis, muscular coat), submucosa (tela submucosa)
Together with the tunica mucosa, the microcirculatory bed and mucosa (tunica mucosa, mucous membrane). The mus-
of the colon plays a central role in the absorptive, secretory cular layer is composed of two layers: longitudinal layer
and protective functions of the colon. Capillary endothelial (stratum longitudinale), reduced in the taenia coli (except
cells have a low proliferative rate and long turnover time, in the vermiform appendix and rectum), and circular layer
thus providing a relatively stable structure within most tis- (stratum circulare). The mucosa is divided into three parts:
sues. The two principal functions of the colon appear to be muscularis mucosae (lamina muscularis mucosae), propria
the storage of faeces before evacuation and high-capacity mucosae (lamina propria mucosae) and epithelium.
water absorption (Standring, 2005; Kachlik, 2006; Kachlik & A thorough and detailed study summarizing the arrange-
Hoch, 2008). ment of the microcirculatory bed in all layers of the large
As for the wall of the large intestine, it is composed of intestine using injection methods on both the macroscopic
five main concentric layers (some of them having several and microscopic level has not yet been performed.
sublayers), which are ordered according to their position Thus, the aim of the study was to describe the microcircu-
from the external surface to the lumen (Wolfram-Gabel lation in the wall of the large intestine in detail by the use
et al. 1986): serosa (tunica serosa, serous coat), subserosa of several methods. For study at the macroscopic level, India
ink injection was used, whereas at the microscopic level,
corrosion casting and histomorphology were applied. Par-
Correspondence ticular attention was paid to the terminology of the
David Kachlik, Third Faculty of Medicine, Charles University in branches and plexuses. A model of the arrangement of the
Prague, Ruská 87, Praha 10, 10000, Czech Republic. blood vessels in the normal (healthy) large intestine was cre-
T: +420267102508; F: +420267102504; E: david.kachlik@lf3.cuni.cz ated for possible comparison with pathological states, e.g.
Accepted for publication 13 November 2009 Crohn’s disease, ulcerative colitis, colorectal cancer, etc.

ª 2010 The Authors


Journal compilation ª 2010 Anatomical Society of Great Britain and Ireland
336 Spatial arrangement of colon wall circulation, D. Kachlik et al.

Materials and methods


Two types of material were used in the study. A total of 142
samples were gathered from 118 cadavers (51 women and 67
men, aged 23–91 years) at the Department of Pathology of the
Third Faculty of Medicine, Charles University in Prague and at
the Královské Vinohrady Faculty Hospital in Prague. Another 21
samples were harvested during the operations of 20 patients (14
women and 6 men, aged 18–67 years) at the Department of Sur-
gery of both affiliations.
Wedge-shaped specimens were cut out equally from all seg-
ments of the large intestine. Each specimen included a 10–15-
cm section of the intestine with the mesocolon and supplying
blood vessels. The source vessel was dissected, incised and cann-
ulated, rinsed with saline (20–25 C) and injected. Two injection
media were used to replace the transparent saline.
1 A solution of black India ink (in a ratio of 2 : 3 with distilled
water, at 20–25 C) was successively injected into the vessel by Fig. 1 The corrosion cast of the vascular bed of the transverse colon
means of hand-controlled pressure. After ligation of the supplying and mesocolon with the Drummond’s marginal artery (arteria
blood vessels, the sample was immersed in an 8% formaldehyde marginalis coli). Bar: 2 cm. AM, arteria marginalis coli; aa, arterial
solution to be fixed for at least 10 days. After fixation it was arcade; vC, vasa centralia; vRL, vasa recta longa.
dissected under a Nikon SMZ-U preparation magnifying glass.
2 A commercial product of the synthetic methylmetacrylate resin, course, branching and relation to the neighbouring
Mercox C1-2B or Mercox C1-2R (Ladd Research, Burlington, VA, structures.
USA). A mixture containing 4 mL of prepolymerized resin and
1 mL of the monomer of methylmetacrylic acid containing
Straight vessels of the large intestine (vasa recta
62.5 mg of the methylmetacrylate paste as an accelerator was
intestini crassi)
made in the syringe and injected. Following injection and the
polymerization of Mercox, a 7.5% solution of potassium The vasa recta are branches from the Drummond’s marginal
hydroxide or 16% solution of nitric acid was used as macerating artery (arteria marginalis coli) or from the most peripheral
agent. The final corrosion cast was blue (if using the potassium (i.e. last) arcades of the colic arteries (see Fig. 1). Running
lye maceration), yellow (if using the blue Mercox and the nitric straight to the intestinal wall, they abruptly change their
acid maceration) or red (if using the red Mercox and the nitric direction when entering the serosa. Within the outermost
acid maceration). layer of the large intestine wall their branches form a fine
Afterwards, 51 samples of the large intestine were studied by intermingled net called the subserous plexus, which is the
scanning electron microscope (SEM). They were sputtered with only contribution of the vasa recta to the vascularization of
gold powder in the 11HD Polaron Series (sputter coater). In the the intestinal wall proper.
SEM, voltages of 2.5 and 10 kV were applied under magnifica-
There are rich anastomoses between individual vessels on
tions of 4–396 to scan the samples (Phillips ESEM XL30 with
both surfaces of the large intestine and no regional differ-
Cambridge Stereoscan 250). For details of the method, see Ahar-
inejad et al. (1992), Kachlik (2006) and Kachlik & Hoch (2008). ences are featured. They are arranged in a loose network of
The terminology used to describe the branches and plexus are transverse meshes bordered by mildly tortuous arteries.
based on the Terminologia Anatomica; the terms are stated in
English and then in Latin (in brackets using italics) (FCAT 1998).
Subserous plexus (plexus subserosus)
Synonyms: subserous arteries and veins (arteriae subserosae
Ethical considerations
et venae subserosae).
The study was approved by the Ethics Commission of the The vasa recta send frequent collaterals along their way,
Third Faculty of Medicine, Charles University in Prague. All starting at their origin from the marginal artery to their ter-
of the samples were harvested with the written informed mination. Before entering the external muscle layer, the
consent of the patients. short vasa recta give off branches to the mesocolic border
of the large intestinal wall. These branches are scattered
like the rays of a star but their short course limits the extent
Results
to which they can supply the intestinal wall. The short vasa
The blood vessels in the wall of the large intestine can recta only supply the area bordering the attachment of the
be divided into the vasa recta, subserous plexus, submu- mesocolon to the intestinal wall.
cous plexus, intermuscular plexus and mucous plexus. The long vasa recta have a characteristic slightly sinuous
Each of them can be described according to its origin, or sinusoid course in the subserous layer. On approaching

ª 2010 The Authors


Journal compilation ª 2010 Anatomical Society of Great Britain and Ireland
Spatial arrangement of colon wall circulation, D. Kachlik et al. 337

the antimesocolic border, they can take an oblique or paral-


lel turn to the intestinal wall or even change direction and VRL

turn back to the mesocolic border. There are rich anastomo-


ses between the long vasa recta, short vasa recta and also
between both types of vessels. There are also anastomoses Ss
between their collateral and terminal branches at the meso-
colic and antimesocolic borders regardless of their localiza-
tion. Their average diameter is approximately 80 lm.
The vessels supplying the mesocolic border and mesocolic
taenia are branches of the short vasa recta. In addition,
there are branches of the long vasa recta or their collaterals
TL
supplying the anterior and posterior surface without any
penetration into the intestinal wall. Finally, there are
3 mm
branches for the distant omental taenia and free taenia,
which are derived from the terminal branches of the long
vasa recta before their penetrating into the intestinal wall. Fig. 2 The long vasa recta longa of the transverse colon submerging
The length of the subserous arteries does not exceed 8 mm, under the free taenia. India ink injection. Bar: 3 mm. Ss, plexus
usually varying between 2 and 4 mm. The subserous arteries subserosus; VRL, vasa recta longa; TL, taenia libera.
always terminate in the same manner. As they approach
any taenia or intestinal border, they bifurcate into a left
and a right branch of equal calibre (30–40 lm) taking a
course parallel to the longitudinal axis of the intestine.
Furthermore, in addition to the above-described branches,
there are muscular and omental branches that are derived
from the vasa recta, their collaterals or anastomoses. The
muscular branches change their direction after a short sub-
serous course, penetrating into the muscular layer (calibre:
30 lm). The branches for the greater omentum run perpen-
dicularly to the longitudinal axis of the intestine and leave
the intestinal wall via the omental taenia.
The subserous plexus sends minor branches to feed the
muscular layer of the intestine. They can be classified as
long and short branches, and are advised to be called long
and short muscular branches (rami musculares longi et bre-
ves). The short branches enter the external (longitudinal)
layer, arranged in the taeniae, and supply it, reaching as Fig. 3 The overview of the vascular bed of the large intestine in the
deep as the intermuscular space. The long branches pass scanning electron microscope. Corrosion cast. Bar: 2 mm. Mc, tunica
through the taeniae and send off branches to feed it. They mucosa; Sm, tunica submucosa; Ms, tunica muscularis.
continue and join or pass the intermuscular plexus and
finally terminate in the internal (circular) muscular layer. In recurrentes) and centripetal move in the direction of the
rare cases, they may reach the submucous plexus. This intestinal lumen and give rise to the mucous plexus. In com-
source of the arterial blood supply for the muscular layer is parison with the other layers of the intestinal wall, the sub-
to be considered of minor importance (see Figs 2–6). mucosa is rather thin (< 100 lm).
The feeding vessels are the long vasa recta. After their
extramural course they turn abruptly and penetrate the
Submucous plexus (plexus submucosus)
whole muscular layer perpendicularly to the longitudinal
The submucous plexus is situated within the submucosa axis of the intestine to reach the submucous plexus. Some
among the loose connective tissue, lymph vessels and ner- branches from the subserous plexus (long muscular
vous submucous plexus of Meissner. The vascular network is branches) may rarely reach the submucous plexus but their
composed of vessels of a large calibre running parallel to contribution to the plexus is negligible.
the longitudinal axis of the intestine. This plexus sends off The centrifugal branches can be divided into several types
branches for the terminal vascularization of the inner layers of arteries depending on their length, branching and termi-
of the intestinal wall. The outgoing vessels follow two nation. The centripetal branches are sent off perpendicu-
opposite directions – centrifugal turn back to the muscular larly to the longitudinal axis of the intestine and run
layer (called recurrent muscular branches; rami musculares directly to the lumen (see Figs 3, 4, 6, 7 and 8).

ª 2010 The Authors


Journal compilation ª 2010 Anatomical Society of Great Britain and Ireland
338 Spatial arrangement of colon wall circulation, D. Kachlik et al.

Fig. 4 The cross-section of the vascular bed of the large intestine in


the scanning electron microscope. Corrosion cast. Bar: 200 lm. Mu,
tunica mucosa; Sm, tunica submucosa; Ms, tunica muscularis; Ss,
plexus subserosus; aR, arteria recta; vR, vena recta. Fig. 6 The scheme of the intramural plexuses in cross-section of the
large intestine wall (freely according to Wolfram-Gabel). MT,
mesocolon transversum; LGC, ligamentum gastrocolicum; TM, tunica
mucosa; TSM, tunica submucosa; SC, stratum circulare; SL, stratum
longitudinale; OM, omentum majus; AO, appendix omentalis, ARL,
arteria recta longa; ARB, arteria recta brevis; PIM, plexus
intermuscularis; PSM, plexus submucosus; PM, plexus mucosus; PSS,
plexus subserosus.

Fig. 5 The external view of the surface of the vascular bed of the
large intestine in the scanning electron microscope. Corrosion cast.
Bar: 2 mm. VR1, VR2, adjacent vasa recta.

Intermuscular plexus (plexus intermuscularis)


Synonyms: plexus muscularis, plexus myentericus. Fig. 7 The longitudinal section of the vascular bed of the large
There is a greater number of feeding vessels that serve as intestine in the scanning electron microscope. Corrosion cast. Bar:
500 lm. Mu, tunica mucosa; SM, tunica submucosa; C, glandulae
a source for the muscular layer; they are issued by the sub-
intestinales = Lieberkühn’s crypts; a, artefacts (extravasates).
mucous plexus as its centrifugal branches, by the subserous
plexus as centripetal branches or emerge directly from the
penetrating vasa recta. According to their length, they can be classified as long,
The centrifugal branches from the submucous plexus are middle and short. The short recurrent muscular branches
the most important source of arterial blood for the muscu- (rami musculares recurrentes breves) terminate exclusively
lar layer of the intestinal wall. They are called the recurrent in the internal (circular) muscular layer without reaching
muscular branches (rami musculares recurrentes plexus sub- the intermuscular plexus. They are very short, ranging from
mucosi). They originate in the submucous layer from trunks 250 to 500 lm. The middle branches (rami musculares recur-
of the vasa recta, their collaterals or from mutual anastomo- rentes medii) supply the internal (circular) muscular layer
ses. Their diameter ranges from 25 to 30 lm. and the intermuscularis plexus, which runs in a perpendicu-

ª 2010 The Authors


Journal compilation ª 2010 Anatomical Society of Great Britain and Ireland
Spatial arrangement of colon wall circulation, D. Kachlik et al. 339

The branches derived from this plexus and from all vessels
passing the muscular layer are called the interfascicular
branches (rami interfasciculares). Their diameter ranges
from 10 to 20 lm and they run rectilinearly between the
muscle fascicles which they supply. There are rich mutual
anastomoses. Finally, they send the fascicular branches
(rami fasciculares), which are 10–15 lm in diameter, into
the muscle fascicles perpendicularly to their longitudinal
axis. Their terminal branches are the precapillary arterioles
anastomosing with each other and forming a terminal arte-
riolar network giving rise to the capillary bed of the muscu-
lar fascicle (see Figs 3, 4 and 6).

Mucous plexus (plexus mucosus)

Fig. 8 The detail of the longitudinal section of the vascular bed of the The entire thickness of the mucosa is regularly juxtaposed
large intestine in the scanning electron microscope. Corrosion cast. by intestinal glands (glandulae intestinales; Lieberkühn’s
Bar: 200 lm. Mu, tunica mucosa; Sm, tunica submucosa; C, crypts). The upper ends of the glands open into the intesti-
glandulae intestinales = Lieberkühn’s crypts; a, artefacts (extravasate). nal lumen and the bases reach as deep as the muscularis
mucosae. The mucous plexus resembles a mosaic because of
its regular dimensions and shape. The diameter of its vessels
lar and rectilinear direction through the circular muscle ranges from 25 to 30 lm. The mucous plexus is fed by the
layer (750–1000 lm). They terminate in the intermuscular mucosal branches from the submucous plexus. They run
plexus, which is parallel to the longitudinal axis of the intes- perpendicularly to the longitudinal axis of the intestine.
tine. Finally, the long branches (rami musculares recurrentes Due to the presence of folds on the mucosal surface, their
longi) have the same orientation as the middle branches course is variable and they can be classified as long and
but reach as far as the muscular bundles of the taeniae short (see Figs 6–8).
(longitudinal muscular layer). Some may even join the sub- The short mucous branches (rami mucosi breves) run to
serous plexus. During their course, they send off branches the segments of mucosa located between two semilunar
for both muscular layers and for the intermuscular plexus, folds. They originate from the adjacent submucous plexus
their length ranging from 1500 to 2000 lm. There are fre- and send off two to four collateral branches. Their length
quent anastomoses between collateral and terminal ranges from 500 to 1000 lm. The long mucous branches
branches of all types of the recurrent muscular branches. (rami mucosi longi) run in the mucosa of the semilunar
The second source of the arterial blood vessels, although folds. Their course is more rectilinear and sometimes slightly
less numerous in branches and less voluminous, is provided flexed. The long mucous branches range in length from 2
by arteries issued centripetally from the subserous plexus to 5 mm. Each branch bifurcates at a variable distance from
(rami musculares plexus subserosi). These can be classified the lumen into two branches of the first order (15 lm in
as long and muscular branches. They originate from either diameter). These branches then send off two or three more
the vasa recta or from their collaterals and anastomoses. branches of second order, respectively. All of these collater-
Although not as significant as the recurrent muscular als successively send the precapillary arterioles (10 lm in
branches from the submucous plexus, these branches con- diamater). The arterioles coil round the bases and bodies of
tribute considerably to the arterial blood supply of all three the intestinal glands and descend as far as the furthermost
taeniae. Their diameter is approximately 25 lm. luminal surface. Some of the arterioles run a straight course
The short muscular branches enter the taeniae (longitudi- but the majority form waves and intermingle with each
nal muscular layer) running perpendicularly to the longitu- other, sending off capillaries. A dense network of capillaries
dinal axis of the intestine and supply them. Some terminal covers the glands, which are embedded in a vascular cush-
branches reach the intermuscularis plexus, being 200 lm ion (see Fig. 8).
long (or 400 lm via the taenia) and helping to feed it. The The luminal surface is covered by capillaries. They change
long muscular branches pass through the longitudinal mus- their direction from perpendicular to horizontal and then
cular layer and send off some nourishing branches. They they turn back and run deep to join a venule. They may also
then join or pass the intermuscular plexus within the inter- curve along the circular opening brim of the gland orifice,
muscular space and terminate in the circular muscular layer. encircling it like rods of a wreath (see Fig. 9).
Their length is usually between 750 and 1500 lm. In rare The wreath-like structures are formed by one to five cap-
cases, they may even reach the submucous plexus and con- illaries and have various widths. The capillaries anastomose
tribute to its blood supply. with each other to encircle the circumference of the gland

ª 2010 The Authors


Journal compilation ª 2010 Anatomical Society of Great Britain and Ireland
340 Spatial arrangement of colon wall circulation, D. Kachlik et al.

Fig. 11 The luminal orifices of the glandulae intestinales (Lieberkühn’s


crypts) of the vascular bed of the large intestine. Corrosion cast. Bar:
Fig. 9 The overview of the vascular bed luminal surface of the large
50 lm.
intestine in the scanning electron microscope. Corrosion cast.
Capillaries encircling the luminal orifice of the glandulae intestinales.
Bar: 100 lm. Feeding capillaries enwrap the walls and encircle the
luminal gland orifice. ing a system of vascular wreaths mutually connected and
merging to form a carpet. The diameter of the gland orifice
varies from 60 to 90 lm and the depth of the gland ranges
from 250 to 300 lm.
The total view of the gland carpet may resemble a honey-
comb (see Fig. 8). The gland orifices are arranged in a hex-
agonal web; the centre of one gland orifice is situated in
the middle of a hexagon and the corners are located in the
orifices of six adjacent glands (see Fig. 11). This strictly regu-
lar disposition organization of the intestinal gland reflects
the arrangement of the large intestine mucosa. The total
width of the mucous plexus varies from 200 to 300 lm.

Discussion
Resin corrosion injections are the most suitable technique
to depict and study the arrangement of blood vessels in the
intestinal wall at both the macroscopic and microscopic
level (Shikata & Shida, 1985; Christofferson & Nilsson, 1988;
Krstić, 1991; Aharinejad et al. 1992; Hossler, 1998). Our stud-
ies confirm this. As for the microcirculatory bed of the wall
of the large intestine, there are several studies reporting
Fig. 10 The overview of the vascular bed luminal surface of the large
the successful application of this technique in animals
intestine in the scanning electron microscope. Corrosion cast. Bar:
200 lm. Hexagons of the bee honeycomb arrangement of glandulae (Shikata & Shida, 1985; Browning & Gannon, 1986; Christ-
intestinales. offerson & Nilsson, 1988; Krstić, 1991; Aharinejad et al.
1992; Skinner et al. 1995; Hossler, 1998; Sangiorgi et al.
orifice. The length of each individual capillary is different, 2007) but only few articles concerning the application in
ranging from a narrow spot, enabling the capillary to humans (Gannon et al. 1984; Sun et al. 1992; Skinner et al.
change the ascending course into the descending course, to 1995; Araki et al. 1996; Fait et al. 1998). In animals, the prin-
one-half of the gland orifice circumference (see Fig. 10). cipal study was published by Shikata & Shida (1985). They
Some capillaries connect adjacent wreathes of vessels, usu- applied this technique in the experimental study of colon
ally in more anastomosing sites. This mosaic (carpet) is iden- anastomosis in healing after the stapler operation using
tical to the SEM picture of the normally-shaped intestinal instruments of various origins in dogs. Gannon et al. (1984)
mucosa. The outline of the glands is maintained mainly by carried out an experiment involving vascular injections fol-
the dense network of the superficially laid capillaries form- lowed by in-vivo microscopy of the laboratory rat large

ª 2010 The Authors


Journal compilation ª 2010 Anatomical Society of Great Britain and Ireland
Spatial arrangement of colon wall circulation, D. Kachlik et al. 341

intestine. Details of the morphological relationship of indi- ularly to the longitudinal axis of the intestine, thus forming
vidual plexuses to the corresponding intestinal wall layers the second striation. Such an arrangement, first described
and the level of their location were reported by Bernardes in detail by Wolfram-Gabel et al. (1984), resembles that
& Patrı́cio (2004), Boulter & Parks (1960), Goerttler (1932), reported by Szyika (1976) in the jejunum and ileum. Apart
Horstmann (1943), Ohtsuka et al. (1988), Wolfram-Gabel & from nourishing the subserous layer, the main purpose of
Maillot (1981) and Wolfram-Gabel et al. (1982, 1983, 1984, the vasa recta is to penetrate the muscular layer. There are
1986). To compare the data of various segments of the gas- several terminal branches penetrating deep into the wall to
trointestinal tube, see studies by Wolfram-Gabel et al. the submucous layer (Griffiths, 1961 reported four main
(1984, 1986); the duodenum was scrutinized by Szyika sites without any detailed data).
(1976) and Wolfram-Gabel et al. (1982), and the small intes- Ernst (1851) observed that the long vasa recta penetrat-
tine and stomach by Barclay & Bentley (1949). ing the muscular layer send off branches supplying it. Later,
The vascular bed of the large intestine, as described Heller (1872) added the description of the blood supply of
above, resembles a similar arrangement of the intramural the muscular layer directly from the subserous plexus (for
arteries in the stomach (Barclay & Bentley, 1949; Gannon more details, see Hou-Jensen, 1931 and Wolf-Heidegger,
et al. 1984) and small intestine (Szyika, 1976). It also reflects 1942). The intermuscular plexus itself is interposed between
the vascular arrangement in the striated muscle, which was the internal (circular) and external (longitudinal) muscular
described by Saunders et al. (1957) as ‘macromesh’ with a layers (arranged in the taeniae in the majority of the large
finer plexus within it called the ‘micromesh’. In the large intestine) in the intermuscular space. It is rather thin but it
intestine, the term ‘micromesh’ can be applied to the supplies the thickest layer of the large intestinal wall. This is
mucous plexus between the epithelium of the mucosa and the reason why there are accessory vessels directly derived
the submucosa. The rich mucous vascular bed was termed from the adjacent plexuses (subserous and submucous).
the ‘carpet’ by Brockis & Moffat (1958) who discovered the These vessels contribute to the supply of the muscle bundles
similarity of the loops around the intestinal glands with the and fibres without interpolating in any further plexus. The
carpet pattern. plexus helps to hold both muscular layers in place. The long
As for the terminology, we followed the terms proposed recurrent muscular branches have the same course as the
by Wolfram-Gabel & Maillot (1981) and Wolfram-Gabel middle branches but reach as far as the longitudinal muscu-
et al. (1982, 1983, 1984, 1986) and added the Latin terms to lar layer (taeniae). Some even join the subserous plexus, as
all of the branches and plexus described (in brackets using stated by Wolfram-Gabel et al. (1984). The second source of
italics) because the Terminologia Anatomica (1998) and the arterial blood vessels, although less frequent in
Terminologia Histologica (2007) do not include any terms branches and less voluminous, is provided by arteries issued
concerning the microcirculatory bed of the intestine (FCAT by the subserous plexus centripetally. Wolfram-Gabel et al.
1998; FICAT, 2008). (1984) called them the ‘arteriae musculares’ but we recom-
As early as 1736, Albinus described the branching of the mend the term muscular branches from subserous plexus
intramural vessels in the intestinal wall but his study was (rami musculares plexus subserosi). As for the mucous
limited to the small intestine. This was proven by the trans- plexus, our results of the diameter of the intestinal gland
lation of his thesis (Albinus, 1736; Kachlik, 2006; Kachlik & orifices (varying from 60 to 90 lm) are similar to those
Hoch, 2008). Bourgery (1839) described the subserous plexus reported by Wolfram-Gabel et al. (1983) (80–100 lm).
as the principal plexus issuing arteries for the deeper layers Al-Fallouji (1984) was the first to emphasize that there
of the intestinal wall. Mellière (1927) assumed the vasa are no regional differences in the arrangement of the intra-
recta to be branches from the marginal artery, opening out mural plexuses of the large intestine. Any segment of the
in the subserous connective tissue into a plexus nourishing large intestine can be used as the terminal end for a postre-
all deeper layers. section anastomosis. There is no morphological background
There is extensive branching of the subserous arteries, for the development of ischaemic consequences after the
especially in anastomotic branches that are rich in the subs- anastomosis of two segments of the large intestine follow-
erous layer and can be divided into anastomoses of the first ing resection. Rather, the factors of primary importance
and second order, respectively. The first-order anastomoses include: the calibre of the colon lumen, width of the colon
are situated either between two collateral branches, wall and the mobility of the colon segment. The danger of
between two terminal branches or between the collateral ischaemia is due to the extensive traction of the mesocolon
and terminal branch of the adjacent vasa recta. Their diam- or the newly anastomosed large intestine.
eter is approximately 50 lm and they are arranged in a reg- The existence of the continuous intramural plexuses
ular network with distances between adjacent vessels from within the whole length of the small and large intestine
1.4 to 2.0 mm. This creates an impression of the continuous allows us to confirm the theory of a compact intestinal intra-
and regular striation. The second-order anastomoses (being mural vascular canal. Such a connection is like one huge
of the same dimensions) are branches of the previous level anastomosis that can replace the blood supply of one source
of anastomoses, situated mostly transversely and perpendic- artery if some disruption in flow occurs. A blockage due to

ª 2010 The Authors


Journal compilation ª 2010 Anatomical Society of Great Britain and Ireland
342 Spatial arrangement of colon wall circulation, D. Kachlik et al.

either iatrogenic (ligation) or pathological (embolization, colon is almost single-layered. He speculated that the capil-
thrombosis, obturation or arteriosclerosis) causes can be lary network of the ascending colon is closely related to the
compensated in varying degrees by the anastomoses, which greater degree of water absorption and electrolyte trans-
allow a change in the direction of blood flow. Especially in port activities compared with those of the sigmoid colon.
the rectum, the theory of the inverted blood flow from the
middle and inferior rectal artery to the network of the supe-
Concluding remarks
rior rectal artery, and even more orally, was suggested by
McGregor (1957) and Sunderland (1942). This theory is piv- This article brings together thorough and comprehensive
otal for the denial of the physiological function of the critical information on the arrangement of the blood supply to the
points. These points exist as places of the interrupted blood large intestine wall. All vascular plexuses are connected in a
supply. In certain cases, the macroscopically visible anasto- long channel running through the whole length of the
moses may be absent. In the otherwise healthy and unaf- intestine. If necessary, it can serve as a huge collateral. This
fected patient, they have no physiological function. collateral is sufficient only in an otherwise non-afflicted
However, in cases of any pathological affliction or embryo- intestine (without developmental defect, immune, vascular
logical discrepancy [e.g. in infant necrotizing colitis, arterio- or connective tissue diseases, etc.). It presents a model that
sclerosis (abdominal angina), venous thrombosis and states can serve as a background for other studies concerning the
with disrupted haemocoagulation], these points indicate changes of the large intestine wall blood supply in various
predisposed sites of vulnerability. pathological states, such as colorectal cancer, inflammatory
The architecture of the capillary network in the large bowel disease, especially Crohn’s disease, etc.
intestine segments was qualitatively described by Aharine-
jad & Lametschwandtner (1992) in rats and guinea pigs, by
Acknowledgements
Browning & Gannon (1986), Sangiorgi et al. (2007) and
Skinner et al. (1995) in rats, and in humans only by Sun Grant support: GAUK 108 ⁄ 1999 ⁄ C, GAUK 25 ⁄ 2001 ⁄ C and GAUK
et al. (1992) in normal tissue, transitional mucosa and ade- 103 ⁄ 2004 ⁄ C. Special thanks to Prof. Alois Lametschwandtner
nocarcinoma, by Skinner et al. (1995) comparing rat and (Department of Organismic Biology, Vascular and Muscle
Research Unit, University of Salzburg, Austria) for the use of the
human colon and by Araki et al. (1996) and Fait et al.
SEM laboratory.
(1998). Interestingly, comparisons to the microvascular
architecture of the small intestine revealed some differ-
ences. Skinner et al. (1995) presented different types of Author contributions
microvascular architecture within the individual villi. He dis-
D.K. – substantial contributions to the conception and design,
cerned a fountain-like arrangement, in which the arterioles performance of the injections, corrosion casting, acquisition of
reach the top of the villus without branching (‘fountain- data or analysis and interpretation of data. V.B. – substantial
type’), a deeply interconnected type (‘step ladder’) and a contributions to the conception and design, performance of the
‘tuft-type’. Unfortunately, this classification cannot be injections, corrosion casting, acquisition of data or analysis and
applied to the large intestine. Browning & Gannon (1986) interpretation of data. J.S. – senior author, final approval of the
described a gradual reduction of both the mucous capillary article.

density and of the average network width towards the


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